Uncoordinated 119 protein controls trafficking of Lck via the Rab11 endosome and is critical for immunological synapse formation

Journal of Immunology

Volumn 183, Issue 3, 2009, Pages 1675-1684

  Gorska, Magdalena M ^a,b   Liang, Qiaoling ^a   Karim, Zunayet ^a   Alam, Rafeul ^a,b  

^a DEPARTMENT OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADAPTOR PROTEIN; GUANOSINE TRIPHOSPHATASE; MOLECULAR MOTOR; MYOSIN; MYOSIN VB; PROTEIN KINASE LCK; RAB11 PROTEIN; UNCLASSIFIED DRUG; UNCOORDINATED 119 PROTEIN; MULTIPROTEIN COMPLEX; MYO5B PROTEIN, RAT; RAB PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; UNC119 PROTEIN, HUMAN; UNC119 PROTEIN, MOUSE;

ARTICLE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; CYTOSKELETON; ENDOSOME; ENZYME ACTIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; ANIMAL; ANTIGEN PRESENTATION; CELL CULTURE; IMMUNOLOGY; LEUKEMIA CELL LINE; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT; RAT; T LYMPHOCYTE;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGEN PRESENTATION; CELLS, CULTURED; CYTOSKELETON; ENDOSOMES; HUMANS; IMMUNOLOGICAL SYNAPSES; JURKAT CELLS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MICE; MULTIPROTEIN COMPLEXES; MYOSINS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RATS; T-LYMPHOCYTES;

EID: 68149165398     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900792     Document Type: Article

References (48)

1. Molina, T. J., K. Kishihara, D. P. Siderovski, W. van Ewijk, A. Narendran, E. Timms, A. Wakeham, C. J. Paige, K. U. Hartmann, A. Veillette, et al. 1992. Profound block in thymocyte development in mice lacking p56lck. Nature 357: 161-164.
2. Straus, D. B., and A. Weiss. 1992. Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 70: 585-593.
3. Reth, M. 1989. Antigen receptor tail clue. Nature 338: 383-384.
4. Iwashima, M., B. A. Irving, N. S. van Oers, A. C. Chan, and A. Weiss. 1994. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science 263: 1136-1139. (Pubitemid 24105959)
5. lck in an infant with severe combined immunodeficiency. J. Clin. Invest. 102: 421-429.
6. Ley, S. C., M. Marsh, C.R. Bebbington, K. Proudfoot, and P. Jordan. 1994. Distinct intracellular localization of Lck and Fyn protein tyrosine kinases in human T lymphocytes. J. Cell Biol. 125: 639-649.
7. Li, Q. J., A. R. Dinner, S. Qi, D. J. Irvine, J. B. Huppa, M. M. Davis, and A. K. Chakraborty. 2004. CD4 enhances T cell sensitivity to antigen by coordinating Lck accumulation at the immunological synapse. Nat. Immunol. 5: 791-799.
8. Cen, O., M. M. Gorska, S. J. Stafford, S. Sur, and R. Alam. 2003. Identification of UNC119 as a novel activator of SRC-type tyrosine kinases. J. Biol. Chem. 278: 8837-8845.
9. Maduro, M., and D. Pilgrim. 1995. Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141: 977-988.
10. Higashide, T., and G. Inana. 1999. Characterization of the gene for HRG4 (UNC119), a novel photoreceptor synaptic protein homologous to unc-119. Genomics 57: 446-450.
11. Gorska, M. M., S. J. Stafford, O. Cen, S. Sur, and R. Alam. 2004. Unc119, a novel activator of Lck/Fyn, is essential for T cell activation. J. Exp. Med. 199: 369-379.
12. Grosshans, B. L., D. Ortiz, and P. Novick. 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. USA 103: 11821-11827.
13. Ullrich, O., S. Reinsch, S. Urbé, M. Zerial, and R. G. Parton. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135: 913-924. (Pubitemid 26403768)
14. Murray, R. Z., J. G. Kay, D. G. Sangermani, and J. L. Stow. 2005. A role for the phagosome in cytokine secretion. Science 310: 1492-1495.
15. Satoh, A. K., J. E. O'Tousa, K. Ozaki, and D. F. Ready. 2005. Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132: 1487-1497.
16. Monks, C. R., B. A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395: 82-86.
17. Morgan, M. M., C. M. Labno, G. A. Van Seventer, M. F. Denny, D. B. Straus, and J. K. Burkhardt. 2001. Superantigen-induced T cell:B cell conjugation is mediated by LFA-1 and requires signaling through Lck, but not ZAP70. J. Immunol. 167: 5708-5718.
18. Holdorf, A. D., K. H. Lee, W. R. Burack, P. M. Allen, and A. S. Shaw. 2002. Regulation of Lck activity by CD4 and CD28 in the immunological synapse. Nat. Immunol. 3: 259-264.
19. Hernández-Hoyos, G., M. K. Anderson, C. Wang, E. V. Rothenberg, and J. Alberola-Ila. 2003. GATA-3 expression is controlled by TCR signals and regulates CD4/CD8 differentiation. Immunity 19: 83-94.
20. Ouyang, W., S. H. Ranganath, K. Weindel, D. Bhattacharya, T. L. Murphy, W. C. Sha, and K. M. Murphy. 1998. Inhibition of Th1 development mediated by GATA-3 through an IL-4-independent mechanism. Immunity 9: 745-755. (Pubitemid 28557602)
21. Naviaux, R. K., E. Costanzi, M. Haas, and I. M. Verma. 1996. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70: 5701-5705.
22. Kuhne, M. R., J. Lin, D. Yablonski, M. N. Mollenauer, L. I. Ehrlich, J. Huppa, M. M. Davis, and A. Weiss. 2003. Linker for activation of T cells, ζ-associated protein-70, and Src homology 2 domain-containing leukocyte protein-76 are required for TCR-induced microtubule-organizing center polarization. J. Immunol. 171: 860-866.
23. Nichols, B. J., A. K. Kenworthy, R. S. Polishchuk, R. Lodge, T. H. Roberts, K. Hirschberg, R. D. Phair, and J. Lippincott-Schwartz. 2001. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153: 529-541.
24. Glebov, O. O., N. A. Bright, and B. J. Nichols. 2006. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat. Cell Biol. 8: 46-54.
25. Gorska, M. M., Q. Liang, S. J. Stafford, N. Goplen, N. Dharajiya, L. Guo, S. Sur, M. Gaestel, and R. Alam. 2007. MK2 controls the level of negative feedback in the NF-kappaB pathway and is essential for vascular permeability and airway inflammation. J. Exp. Med. 204: 1637-1652.
26. 30 of Rab5 lead to loss-of-function as well as gain-of-function phenotype. Biochem. J. 355: 681-689.
27. lck translocation to the T cell immunological synapse following agonist and antagonist stimulation. Immunity 17: 809-822.
28. Thoulouze, M. I., N. Sol-Foulon, F. Blanchet, A. Dautry-Varsat, O. Schwartz, and A. Alcover. 2006. Human immunodeficiency virus type-1 infection impairs the formation of the immunological synapse. Immunity 24: 547-561.
29. Sönnichsen, B., S. De Renzis, E. Nielsen, J. Rietdorf, and M. Zerial. 2000. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149: 901-914.
30. Balasubramanian, N., D. W. Scott, J. D. Castle, J. E. Casanova, and M. A. Schwartz. 2007. Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nat. Cell Biol. 9: 1381-1391.
31. Lapierre, L. A., R. Kumar, C. M. Hales, J. Navarre, S. G. Bhartur, J. O. Burnette, D. W. Provance, J. A. Mercer, M. Bähler, and J. R. Goldenring. 2001. Myosin vb is associated with plasma membrane recycling systems. Mol. Biol. Cell 12: 1843-1857.
32. lck travels to the plasma membrane via the exocytic pathway. J. Cell Biol. 145: 457-468.
33. Haller, C., S. Rauch, and O. T. Fackler. 2007. HIV-1 Nef employs two distinct mechanisms to modulate Lck subcellular localization and TCR induced actin remodeling. PLoS ONE 2: e1212.
34. Park, J., B. S. Lee, J. K. Choi, R. E. Means, J. Choe, and J. U. Jung. 2002. Herpesviral protein targets a cellular WD repeat endosomal protein to downregulate T lymphocyte receptor expression. Immunity 17: 221-233.
35. Antón, O., A. Batista, J. Millán, L. Andrés-Delgado, R. Puertollano, I. Correas, and M. A. Alonso. 2008. An essential role for the MAL protein in targeting Lck to the plasma membrane of human T lymphocytes. J. Exp. Med. 205: 3201-3213.
36. +-ATPase. Am. J. Physiol. 277: 361-372.
37. Park, M., E. C. Penick, J. G. Edwards, J. A. Kauer, and M. D. Ehlers. 2004. Recycling endosomes supply AMPA receptors for LTP. Science 305: 1972-1975.
38. 2 integrin, LFA-1, during leukocyte chemotaxis. Mol. Biol. Cell 16: 5793-5803.
39. Kobayashi, A., T. Higashide, D. Hamasaki, S. Kubota, H. Sakuma, W. An, T. Fujimaki, M. J. McLaren, R. G. Weleber, and G. Inana. 2000. HRG4 (UNC119) mutation found in cone-rod dystrophy causes retinal degeneration in a transgenic model. Invest. Ophthalmol. Vis. Sci. 41: 3268-32677.
40. Ang, A. L., T. Taguchi, S. Francis, H. Fölsch, L.J. Murrells, M. Pypaert, G. Warren, and I. Mellman. 2004. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J. Cell Biol. 167: 531-543.
41. Ménager, M. M., G. Ménasché, M. Romao, P. Knapnougel, C. H. Ho, M. Garfa, G. Raposo, J. Feldmann, A. Fischer, and G. de Saint Basile. 2007. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol. 8: 257-267.
42. Ménasché, G., E. Pastural, J. Feldmann, S. Certain, F. Ersoy, S. Dupuis, N. Wulffraat, D. Bianchi, A. Fischer, F. Le Deist, and G. de Saint Basile. 2000. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat. Genet. 25: 173-176.
43. Feldmann, J., I. Callebaut, G. Raposo, S. Certain, D. Bacq, C. Dumont, N. Lambert, M. Ouachée-Chardin, G. Chedeville, H. Tamary, et al. 2003. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 115: 461-473.
44. Dabbeekeh, J. T., S. L. Faitar, C. P. Dufresne, and J. K. Cowell. 2007. The EVI5 TBC domain provides the GTPase-activating protein motif for RAB11. Oncogene 26: 2804-2808.
45. Fuchs, E., A. K. Haas, R. A. Spooner, S. Yoshimura, J. M. Lord, and F. A. Barr. 2007. Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways. J. Cell Biol. 177: 1133-1143.
46. Westlake, C. J., J. R. Junutula, G. C. Simon, M. Pilli, R. Prekeris, R. H. Scheller, P. K. Jackson, and A. G. Eldridge. 2007. Identification of Rab11 as a small GTPase binding protein for the Evi5 oncogene. Proc. Natl. Acad. Sci. USA 104: 1236-1241.
47. Shirane, M., and K. I. Nakayama. 2006. Protrudin induces neurite formation by directional membrane trafficking. Science 314: 818-821.
48. Sechi, A. S., and J. Wehland. 2004. Interplay between TCR signalling and actin cytoskeleton dynamics. Trends Immunol. 25: 257-265.